Evidence for admixture and rapid evolution during glacial climate change in an alpine specialist

The pace of current climate change is expected to be problematic for
alpine flora and fauna, as their adaptive capacity may be limited by small
population size. Yet despite substantial genetic drift following
post-glacial recolonization of alpine habitats, alpine species are notable
for their success in surviving highly heterogeneous environments.
Population genomic analyses demonstrating how alpine species have adapted
to novel environments with limited genetic diversity remain rare, yet are
important in understanding the potential for species to respond to
contemporary climate change. In this study, we explored the evolutionary
history of alpine ground beetles in the Nebria ingens complex, including
the demographic and adaptive changes that followed the last glacier
retreat. We first tested alternative models of evolutionary divergence in
the species complex. Using the millions of genome-wide SNP markers from
hundreds of beetles, we found evidence that the Nebria ingens complex has
been formed by past admixture of lineages responding to glacial cycles.
Recolonization of alpine sites involved a distributional range shift to
higher elevation, which was accompanied by a reduction in suitable habitat
and the emergence of complex spatial genetic structure. We tested several
possible genetic pathways involved in the adaptation to heterogeneous
local environments using whole genome scan and genotype-environment
association approach. From the identified genes, we found enriched
functions broadly associated with abiotic stress responses, with strong
evidence for adaptation to hypoxia-related pathways. The results
demonstrate that despite rapid environmental changes, alpine beetles in
the N. ingens complex have shown rapid physiological evolution.